XBP1 mitigates aminoglycoside-induced endoplasmic reticulum stress and neuronal cell death

Cell Death and Disease

Volumn 6, Issue 5, 2015, Pages

  Oishi, N ^a,c,d   Duscha, S ^b,d   Boukari, H ^b,d   Meyer, M ^b   Xie, J ^a   Wei, G ^a   Schrepfer, T ^a,b   Roschitzki, B ^b   Boettger, E C ^b   Schacht, J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c KEIO UNIVERSITY   (Japan)

^d CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOGLYCOSIDE; CCAAT ENHANCER BINDING PROTEIN; GENTAMICIN; GLUCOSE REGULATED PROTEIN 94; PROTEOME; TAUROURSODEOXYCHOLIC ACID; TRANSCRIPTOME; X BOX BINDING PROTEIN 1; CEBPA PROTEIN, HUMAN; DNA BINDING PROTEIN; MEMBRANE PROTEIN; REGULATORY FACTOR X TRANSCRIPTION FACTOR; TAUROCHENODEOXYCHOLIC ACID; TRANSCRIPTION FACTOR; XBP1 PROTEIN, HUMAN; XBP1 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL DENSITY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FEMALE; HAIR CELL; HEARING; HIGH FREQUENCY HEARING LOSS; IN VITRO STUDY; IN VIVO STUDY; MALE; MAMMAL CELL; MOUSE; NERVE CELL; NONHUMAN; OTOTOXICITY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FOLDING; RNA ANALYSIS; RNA SPLICING; SENSORY NERVE CELL; SPIRAL GANGLION; UNFOLDED PROTEIN RESPONSE; UPREGULATION; ANIMAL; CBA MOUSE; CELL LINE; CHEMICALLY INDUCED; COCHLEAR HAIR CELL; CYTOLOGY; DRUG EFFECTS; ENDOPLASMIC RETICULUM; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROTEIN SYNTHESIS; PROTEOSTASIS DEFICIENCY;

ANIMALS; CCAAT-ENHANCER-BINDING PROTEINS; CELL LINE; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENTAMICINS; HAIR CELLS, AUDITORY; HEARING LOSS, HIGH-FREQUENCY; HEK293 CELLS; HUMANS; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED CBA; NEURONS; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; PROTEOSTASIS DEFICIENCIES; REGULATORY FACTOR X TRANSCRIPTION FACTORS; RNA SPLICING; SPIRAL GANGLION; TAUROCHENODEOXYCHOLIC ACID; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE; X-BOX BINDING PROTEIN 1;

EID: 84970920294     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2015.108     Document Type: Article

References (67)

1. Drummond DA, Wilke CO. Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 2008;134:341-352.
2. Goltermann L, Good L, Bentin T. Chaperonins fight aminoglycoside-induced protein misfolding and promote short-term tolerance in Escherichia coli. J Biol Chem 2013;288:10483-10489.
3. Prostko CR, Brostrom MA, Malara EM, Brostrom CO. Phosphorylation of eukaryotic initiation factor (eIF) 2 alpha and inhibition of eIF-2B in GH3 pituitary cells by perturbants of early protein processing that induce GRP78. J Biol Chem 1992;267:16751-16754.
4. Shi Y, Vattem KM, Sood R, An J, Liang J, Stramm L et al. Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol Cell Biol 1998;18:7499-7509.
5. Tirasophon W, Welihinda AA, Kaufman RJ. A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes Dev 1998;12:1812-1824.
6. Haze K, Yoshida H, Yanagi H, Yura T, Mori K. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 1999;10:3787-3799.
7. Yoshida H, Okada T, Haze K, Yanagi H, Yura T, Negishi M et al. ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response. Mol Cell Biol 2000;20:6755-6767.
8. Shen J, Chen X, Hendershot L, Prywes R. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 2002;3:99-111.
9. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2000;2:326-332.
10. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005;74:739-789.
11. Zhang K, Kaufman RJ. The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 2006;66:S102-S109.
12. Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 2012;13:89-102.
13. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 2000;101:249-258.
14. Yoshida H, Matsui T, Hosokawa N, Kaufman RJ, Nagata K, Mori K. A time-dependent phase shift in the mammalian unfolded protein response. Dev Cell 2003;4:265-271.
15. Lin JH, Li H, Yasumura D, Cohen HR, Zhang C, Panning B et al. IRE1 signaling affects cell fate during the unfolded protein response. Science 2007;318:944-949.
16. Haynes CM, Titus EA, Cooper AA. Degradation of misfolded proteins prevents ER derived oxidative stress and cell death. Mol Cell 2004;15:767-776.
17. Edelmann P, Gallant J. Mistranslation in E. coli. Cell 1977;10:131-137.
18. Palmer E, Wilhelm JM. Mistranslation in a eucaryotic organism. Cell 1978;13:329-334.
19. Palmer E, Wilhelm JM, Sherman F. Phenotypic suppression of nonsense mutants in yeast by aminoglycoside antibiotics. Nature 1979;277:148-150.
20. Stansfield I, Jones KM, Herbert P, Lewendon A, Shaw WV, Tuite MF. Missense translation errors in Saccharomyces cerevisiae. J Mol Biol 1998;282:13-24.
21. Wilhelm JM, Pettitt SE, Jessop JJ. Aminoglycoside antibiotics and eukaryotic protein synthesis: structure-function relationships in the stimulation of misreading with a wheat embryo system. Biochem 1978;17:1143-1149.
22. Buchanan JH, Stevens A, Sidhu J. Aminoglycoside antibiotic treatment of human fibroblasts: intracellular accumulation, molecular changes and the loss of ribosomal accuracy. Eur J Cell Biol 1987;43:141-147.
23. Abraham AK, Pihl A. Effect of protein synthesis inhibitors on the fidelity of translation in eukaryotic systems. Biochim Biophys Acta 1983;741:197-203.
24. Burke JF, Mogg AE. Suppression of a nonsense mutation in mammalian cells in vivo by the aminoglycoside antibiotics G-418 and paromomycin. Nucleic Acids Res 1985;13:6265-6272.
25. Howard M, Frizzell RA, Bedwell DM. Aminoglycoside antibiotics restore CFTR function by overcoming premature stop mutations. Nat Med 1996;2:467-469.
26. Bedwell DM, Kaenjak A, Benos DJ, Bebok Z, Bubien JK, Hong J et al. Suppression of a CFTR premature stop mutation in a bronchial epithelial cell line. Nat Med 1997;3:1280-1284.
27. Nudelman I, Rebibo-Sabbah A, Shallom-Shezifi D, Hainrichson M, Stahl I, Ben-Yosef T et al. Redesign of aminoglycosides for treatment of human genetic diseases caused by premature stop mutations. Bioorg Med Chem Lett 2006;16:6310-6315.
28. Jin QH, Zhao B, Zhang XJ. Cytochrome c release and endoplasmic reticulum stress are involved in caspase-dependent apoptosis induced by G418. Cell Mol Life Sci 2004;61:1816-1825.
29. Quiros Y, Vicente-Vicente L, Morales AI, López-Novoa JM, López-Hernández FJ. An integrative overview on the mechanisms underlying the renal tubular cytotoxicity of gentamicin. Toxicol Sci 2011;119:245-256.
30. Forge A, Schacht J. Aminoglycoside antibiotics. Audiol Neurootol 2000;5:3-22.
31. Kass JS, Shandera WX. Nervous system effects of antituberculosis therapy. CNS drugs 2010;24:655-667.
32. Tan J, Shepherd RK. Aminoglycoside-induced degeneration of adult spiral ganglion neurons involves differential modulation of tyrosine kinase B and p75 neurotrophin receptor signaling. Am J Pathol 2006;169:528-543.
33. Jeong SW, Kim LS, Hur D, Bae WY, Kim JR, Lee JH. Gentamicin-induced spiral ganglion cell death: apoptosis mediated by ROS and the JNK signaling pathway. Acta Otolaryngol 2010;130:670-678.
34. Hinojosa R, Lerner SA. Cochlear neural degeneration without hair cell loss in two patients with aminoglycoside ototoxicity. J Infect Dis 1987;156:449-455.
35. Sone M, Schachern PA, Paparella MM. Loss of spiral ganglion cells as primary manifestation of aminoglycoside ototoxicity. Hear Res 1998;115:217-223.
36. Wu WJ, Sha SH, McLaren JD, Kawamoto K, Raphael Y, Schacht J. Aminoglycoside ototoxicity in adult CBA, C57BL and BALB mice and the Sprague-Dawley rat. Hear Res 2001;158:165-178.
37. Reimold AM, Etkin A, Clauss I, Perkins A, Friend DS, Zhang J et al. An essential role in liver development for transcription factor XBP-1. Genes Dev 2000;14:152-157.
38. Southern PJ, Berg P. Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter. J Mol Appl Genet 1982;1:327-341.
39. Takano M, Okuda M, Yasuhara M, Hori R. Cellular toxicity of aminoglycoside antibiotics in G418-sensitive and -resistant LLC-PK1 cells. Pharm Res 1994;11:609-615.
40. Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM, Bruford EA et al. Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 2009;14:105-111.
41. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 2000;6:1099-1108.
42. Manuvakhova M, Keeling K, Bedwell DM. Aminoglycoside antibiotics mediate context dependent suppression of termination codons in a mammalian translation system. RNA 2000;6:1044-1055.
43. Schneider-Poetsch T, Ju J, Eyler DE, Dang Y, Bhat S, Merrick WC et al. Inhibition of eukaryotic translation elongation by cycloheximide and lactimidomycin. Nat Chem Biol 2010;6:209-217.
44. Wang Y, Shen J, Arenzana N, Tirasophon W, Kaufman R J, Prywes R. Activation of ATF6 and an ATF6 DNA Binding Site by the Endoplasmic Reticulum Stress Response. R. J Biol Chem 2000;275:27013-27020.
45. Yoshida H, Haze K, Yanagi H, Yura T, Mori K. Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins; involvement of basic leucine zipper transcription factors. J Biol Chem 1998;273:33741-33749.
46. Anderson P, Kedersha N. Stressful initiations. J Cell Sci 2002;115:3227-3234.
47. Shulman E, Belakhov V, Wei G, Kendall A, Meyron-Holtz EG, Ben-Shachar D et al. Designer aminoglycosides that selectively inhibit cytoplasmic rather than mitochondrial ribosomes show decreased ototoxicity: a strategy for the treatment of genetic diseases. J Biol Chem 2014;289:2318-2330.
48. Xie J, Talaska AE, Schacht J. New developments in aminoglycoside therapy and ototoxicity. Hear Res 2011;281:28-37.
49. Geisse S, Voedisch B. Transient expression technologies: past, present, and future. Methods Mol Biol 2012;899:203-219.
50. Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011;334:1081-1086.
51. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004;306:457-461.
52. Francis SP, Katz J, Fanning KD, Harris KA, Nicholas BD, Lacy M, Pagana J, Agris PF, Shin JB. A novel role of cytosolic protein synthesis inhibition in aminoglycoside ototoxicity. J Neurosci 2013;33:3079-3093.
53. Taleb M, Brandon CS, Lee FS, Harris KC, Dillmann WH, Cunningham LL. Hsp70 inhibits aminoglycoside-induced hearing loss and cochlear hair cell death. Cell Stress Chaperones 2009;14:427-437.
54. Jiang H, Sha SH, Forge A, Schacht J. Caspase-independent pathways of hair cell death induced by kanamycin in vivo. Cell Death Differ 2006;13:20-30.
55. Fujinami Y, Mutai H, Mizutari K, Nakagawa S, Matsunaga T. A novel animal model of hearing loss caused by acute endoplasmic reticulum stress in the cochlea. J Pharmacol Sci 2012;118:363-372.
56. Peyrou M, Hanna PE, Cribb AE. Cisplatin, gentamicin, and p-aminophenol induce markers of endoplasmic reticulum stress in the rat kidneys. Toxicol Sci 2007;99:346-353.
57. Kujawa SG, Liberman MC. Adding insult to injury: cochlear nerve degeneration after temporary. noise-induced hearing loss. J Neurosci 2009;29:14077-14085.
58. Carrell RW, Lomas DA. Conformational disease. Lancet 1997;350:134-138.
59. Gidalevitz T, Kikis EA, Morimoto RI. A cellular perspective on conformational disease: the role of genetic background and proteostasis networks. Curr Opin Struct Biol 2010;20:23-32.
60. Matt T, Ng CL, Lang K, Sha SH, Akbergenov R, Shcherbakov D et al. Dissociation of antibacterial activity and aminoglycoside ototoxicity in the 4-monosubstituted 2-deoxystreptamine apramycin. Proc Natl Acad Sci USA 2012;109:10984-10989.
61. Salas-Marco J, Bedwell DM. Discrimination between defects in elongation fidelity and termination efficiency provides mechanistic insights into translational readthrough. J Mol Biol 2005;348:801-815.
62. Kramer EB, Vallabhaneni H, Mayer LM, Farabaugh PJ. A comprehensive analysis of translational missense errors in the yeast Saccharomyces cerevisiae. RNA 2010;16:1797-1808.
63. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001;29:e45.
64. Oishi N, Kendall A, Schacht J. Metformin protects against gentamicin-induced hair cell death in vitro but not ototoxicity in vivo. Neurosci Lett 2014;583:65-69.
65. Oishi N, Chen FQ, Zheng HW, Sha SH. Intra-tympanic delivery of short interfering RNA into the adult mouse cochlea. Hear Res 2013;296:36-41.
66. Zhao LJ, Subramanian T, Zhou Y, Chinnadurai G. Acetylation by p300 regulates nuclear localization and function of the transcriptional corepressor CtBP2. J Biol Chem 2006;281:4183-4189.
67. Tong M, Brugeaud A, Edge AS. Regenerated synapses between postnatal hair cells and auditory neurons. J Assoc Res Otolaryngol 2013;14:321-329.